Skip to main content
SpringerLink
Log in

Chemical Tools for Temporally and Spatially Resolved Mass Spectrometry-Based Proteomics

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Accurate measurements of the abundances, synthesis rates and degradation rates of cellular proteins are critical for understanding how cells and organisms respond to changes in their environments. Over the past two decades, there has been increasing interest in the use of mass spectrometry for proteomic analysis. In many systems, however, protein diversity as well as cell and tissue heterogeneity limit the usefulness of mass spectrometry-based proteomics. As a result, researchers have had difficulty in systematically identifying proteins expressed within specified time intervals, or low abundance proteins expressed in specific tissues or in a few cells in complex microbial systems. In this review, we present recently-developed tools and strategies that probe these two subsets of the proteome: proteins synthesized during well-defined time intervals—temporally resolved proteomics—and proteins expressed in predetermined cell types, cells or cellular compartments—spatially resolved proteomics—with a focus on chemical and biological mass spectrometry-based methodologies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. Aebersold, R., and M. Mann. Mass spectrometry-based proteomics. Nature 422:198–207, 2003.

    Article  CAS  PubMed  Google Scholar 

  2. Agard, N., J. Prescher, and C. Bertozzi. A strain-promoted [3+2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J. Am. Chem. Soc. 126:15046–15047, 2004.

    Article  CAS  PubMed  Google Scholar 

  3. Ahrens, C. H., E. Brunner, E. Qeli, K. Basler, and R. Aebersold. Generating and navigating proteome maps using mass spectrometry. Nat. Rev. Mol. Cell Biol. 11:789–801, 2010.

    Article  CAS  PubMed  Google Scholar 

  4. Bantscheff, M., M. Schirle, G. Sweetman, J. Rick, and B. Kuster. Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 389:1017–1031, 2007.

    Article  CAS  PubMed  Google Scholar 

  5. Bantscheff, M., S. Lemeer, M. H. Savitski, and B. Kuster. Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal. Bioanal. Chem. 404:939–965, 2012.

    Article  CAS  PubMed  Google Scholar 

  6. Beatty, K., F. Xie, Q. Wang, and D. Tirrell. Selective dye-labeling of newly synthesized proteins in bacterial cells. J. Am. Chem. Soc. 127:14150–14151, 2005.

    Article  CAS  PubMed  Google Scholar 

  7. Beatty, K., J. Liu, F. Xie, D. Dieterich, E. Schuman, Q. Wang, and D. Tirrell. Fluorescence visualization of newly synthesized proteins in mammalian cells. Angew. Chem. Int. Ed. 45:7364–7367, 2006.

    Article  CAS  Google Scholar 

  8. Black, D. L. Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 103:367–370, 2000.

    Article  CAS  PubMed  Google Scholar 

  9. Boisvert, F. M., Y. W. Lam, D. Lamont, and A. I. Lamond. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 9:457–470, 2010.

    Article  CAS  PubMed  Google Scholar 

  10. Brunet, I., C. Weinl, M. Piper, A. Trembleau, M. Volovitch, W. Harris, A. Prochiantz, and C. Holt. The transcription factor Engrailed-2 guides retinal axons. Nature 438:94–98, 2005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Corthals, G. L., V. C. Wasinger, D. F. Hochstrasser, and J. C. Sanchez. The dynamic range of protein expression: a challenge for proteomic research. Electrophoresis 21:1104–1115, 2000.

    Article  CAS  PubMed  Google Scholar 

  12. Cox, J., N. Neuhauser, A. Michalski, R. A. Scheltema, J. V. Olsen, and M. Mann. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10:1794–1805, 2011.

    Article  CAS  PubMed  Google Scholar 

  13. Deal, R. B., and S. Henikoff. A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev. Cell 18:1030–1040, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Deal, R. B., J. G. Henikoff, and S. Henikoff. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328:1161–1164, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. de Godoy, L. M. F., J. V. Olsen, J. Cox, M. L. Nielsen, N. C. Hubner, F. Fröhlich, T. C. Walther, and M. Mann. Comprehensive mass spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455:1251–1254, 2008.

    Article  PubMed  Google Scholar 

  16. de Sousa Abreu, R., L. O. Penalva, E. M. Marcotte, and C. Vogel. Global signatures of protein and mRNA expression levels. Mol. Biosyst. 5:1512–1526, 2009.

  17. Dieterich, D. C., A. J. Link, J. Graumann, D. A. Tirrell, and E. M. Schuman. Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc. Natl. Acad. Sci. USA 103:9482–9487, 2006.

    Article  CAS  PubMed  Google Scholar 

  18. Dieterich, D. C., J. Hodas, G. Gouzer, I. Shadrin, J. Ngo, A. Triller, D. Tirrell, and E. Schuman. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 13:897–905, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Eichelbaum, K., M. Winter, M. B. Diaz, S. Herzig, and J. Krijgsveld. Selective enrichment of newly synthesized proteins for quantitative secretome analysis. Nat. Biotechnol. 30:984–990, 2012.

    Article  CAS  PubMed  Google Scholar 

  20. Essader, A. S., B. J. Cargile, J. L. Bundy, and J. L. Stephenson. A comparison of immobilized pH gradient isoelectric focusing and strong cation-exchange chromatography as a first dimension in shotgun proteomics. Proteomics 5:24–34, 2005.

    Article  CAS  PubMed  Google Scholar 

  21. Fredens, J., K. Engholm-Keller, A. Giessing, D. Pultz, M. R. Larsen, P. Højrup, J. Møller-Jensen, and N. J. Færgeman. Quantitative proteomics by amino acid labeling in C. elegans. Nat. Methods 8:845–847, 2011.

    Article  CAS  PubMed  Google Scholar 

  22. Friedel, C. C., L. Dolken, Z. Ruzsics, U. H. Koszinowski, and R. Zimmer. Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res. 37:e115, 2009.

    Article  PubMed Central  PubMed  Google Scholar 

  23. Gay, L., M. R. Miller, P. B. Ventura, V. Devasthali, Z. Vue, H. L. Thompson, S. Temple, H. Zong, M. D. Cleary, K. Stankunas, and C. Q. Doe. Mouse TU tagging: a chemical/genetic intersectional method for purifying cell type-specific nascent RNA. Genes Dev. 27:98–115, 2013.

    Article  CAS  PubMed  Google Scholar 

  24. Golebiowski, F., I. Matic, M. H. Tatham, C. Cole, Y. Yin, A. Nakamura, J. Cox, G. J. Barton, M. Mann, and R. T. Hay. System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2:ra24, 2009.

    Google Scholar 

  25. Grammel, M., M. M. Zhang, and H. C. Hang. Orthogonal alkynyl-amino acid reporter for selective labeling of bacterial proteomes during infection. Angew. Chem. Int. Ed. 49:5970–5974, 2010.

    Article  CAS  Google Scholar 

  26. Gresham, D., M. J. Dunham, and D. Botstein. Comparing whole genomes using DNA microarrays. Nat. Rev. Genet. 9:291–302, 2008.

    Article  CAS  PubMed  Google Scholar 

  27. Gygi, S. P., B. Rist, S. A. Gerber, F. Turecek, M. H. Gelb, and R. Aebersold. Quantitative analysis of complex protein mixtures using isotope coded affinity tags. Nat. Biotechnol. 17:994–999, 1999.

    Article  CAS  PubMed  Google Scholar 

  28. Henry, G. L., F. P. Davis, S. Picard, and S. R. Eddy. Cell type-specific genomics of Drosophila neurons. Nucleic Acids Res. 40:9691–9704, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Hinz, F. I., D. C. Dieterich, D. A. Tirrell, and E. M. Schuman. Noncanonical amino acid labeling in vivo to visualize and affinity purify newly synthesized proteins in larval zebrafish. ACS Chem. Neurosci. 3:40–49, 2012.

    Article  CAS  PubMed  Google Scholar 

  30. Hodas, J. J. L., A. Nehring, N. Höche, M. J. Sweredoski, R. Pieolt, S. Hess, D. A. Tirrell, D. C. Dieterich, and E. M. Schuman. Dopaminergic modulation of the hippocampal neuropil proteome identified by bioorthogonal noncanonical amino acid tagging (BONCAT). Proteomics 12:2464–2476, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Howden, A. J. M., V. Geoghegan, K. Katsch, G. Efstathiou, B. Bhushan, O. Boutureira, B. Thomas, D. C. Trudgian, B. M. Kessler, D. C. Deiterich, B. G. Davis, and O. Acuto. QuaNCAT: quantitating proteome dynamics in primary cells. Nat. Methods 10:343–346, 2013.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Hughes, C., and J. Krijgsveld. Developments in quantitative mass spectrometry for the analysis of proteome dynamics. Trends Biotechnol. 30:668–676, 2012.

    Article  CAS  PubMed  Google Scholar 

  33. Huo, Y., V. Iadevaia, Z. Yao, I. Kelly, S. Cosulich, S. Guichard, L. J. Foster, and C. G. Proud. Stable isotope-labelling analysis of the impact of inhibition of the mammalian target of rapamycin on protein synthesis. Biochem. J. 444:141–151, 2012.

    Article  CAS  PubMed  Google Scholar 

  34. Kaller, M., S. T. Liffers, S. Oeljeklaus, K. Kuhlmann, S. Röh, R. Hoffmann, B. Warscheid, and H. Hermeking. Genome-wide characterization of miR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Mol. Cell. Proteomics 10:M111.010462, 2011.

    Google Scholar 

  35. Khidekel, N., S. B. Ficarro, E. C. Peters, and L. C. Hsieh-Wilson. Exploring the O-GlcNAc proteome: direct identification of O-GlcNAc-modified proteins. Proc. Natl. Acad. Sci. USA 101:13132–13137, 2004.

    Article  CAS  PubMed  Google Scholar 

  36. Kiick, K. L., E. Saxon, D. A. Tirrell, and C. R. Bertozzi. Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation. Proc. Natl. Acad. Sci. USA 99:19–24, 2002.

    Article  CAS  PubMed  Google Scholar 

  37. Kraft-Terry, S. D., and H. E. Gendelman. Proteomic biosignatures for monocyte-macrophage differentiation. Cell. Immunol. 271:239–255, 2011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Kramer, G., R. R. Sprenger, M. A. Nessen, W. Roseboom, D. Speijer, L. de Jong, M. J. de Mattos, J. Back, and C. G. de Koster. Proteome-wide alterations in Escherichia coli translation rates upon anaerobiosis. Mol. Cell. Proteomics 9:2508–2516, 2010.

    Article  CAS  PubMed  Google Scholar 

  39. Kramer, G., R. R. Sprenger, J. Back, H. L. Dekker, M. A. Nessen, J. H. van Maarseveen, L. J. de Koning, K. J. Hellingwerf, D. de Jong, and C. G. de Koster. Identification and quantitation of newly synthesized proteins in Escherichia coli by enrichment of azidohomoalanine-labeled peptides with diagonal chromatography. Mol. Cell. Proteomics 8:1599–1611, 2009.

    Article  CAS  PubMed  Google Scholar 

  40. Krijgsveld, J., R. F. Ketting, T. Mahmoudi, J. Johansen, M. Artal-Sanz, C. P. Verrijzer, R. H. A. Plasterk, and A. J. R. Heck. Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nat. Biotechnol. 21:927–931, 2003.

    Article  CAS  PubMed  Google Scholar 

  41. Krüger, M., M. Moser, S. Ussar, I. Thievessen, C. A. Luber, F. Forner, S. Schmidt, S. Zanivan, R. Fässler, and M. Mann. SILAC mouse for quantitative proteomics uncovers Kindlin-3 as an essential factor for red blood cell function. Cell 134:353–364, 2008.

    Article  PubMed  Google Scholar 

  42. Lam, Y. W., A. I. Lamond, M. Mann, and J. S. Andersen. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 17:749–760, 2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Larance, M., A. P. Bailly, E. Pourkarimi, R. T. Hay, G. Buchanan, S. Coulthurst, D. P. Xirodimas, A. Gartner, and A. I. Lamond. Stable isotope labeling with amino acids in nematodes. Nat. Methods 8:849–851, 2011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Larrabee, K. L., J. O. Phillips, G. J. Williams, and A. R. Larrabee. The relative rates of protein synthesis and degradation in a growing culture of Escherichia coli. J. Biol. Chem. 255:4125–4130, 1980.

    CAS  PubMed  Google Scholar 

  45. Link, A. J., M. K. S. Vink, N. J. Agard, J. A. Prescher, C. R. Bertozzi, and D. A. Tirrell. Discovery of aminoacyl-tRNA synthetase activity through cell-surface display of noncanonical amino acids. Proc. Natl. Acad. Sci. USA 103:10180–10185, 2006.

    Article  CAS  PubMed  Google Scholar 

  46. Liu, J., Y. Xu, D. Stoleru, and A. Salic. Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin. Proc. Natl. Acad. Sci. USA 109:413–418, 2012.

    Article  CAS  PubMed  Google Scholar 

  47. Liu, K., P. Y. Yang, Z. Na, and S. Q. Yao. Dynamic monitoring of newly synthesized proteomes: up-regulation of myristoylated protein kinase A during butyric acid induced apoptosis. Angew. Chem. Int. Ed. 50:6776–6781, 2001.

    Article  Google Scholar 

  48. Mahdavi, A., T. H. Segall-Shaprio, S. Kou, G. A. Jindal, K. G. Hoff, S. Liu, M. Chitsaz, R. F. Ismagilov, J. J. Silberg, and D. A. Tirrell. A genetically encoded AND gate for cell-targeted metabolic labeling of proteins. J. Am. Chem. Soc. 135:2979–2982, 2013.

    Article  CAS  PubMed  Google Scholar 

  49. Maier, T., M. Guell, and L. Serrano. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 583:3966–3973, 2009.

    Article  CAS  PubMed  Google Scholar 

  50. Mann, M. Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 7:952–958, 2006.

    Article  CAS  PubMed  Google Scholar 

  51. Martell, J. D., T. J. Deerinck, Y. Sancak, T. L. Poulos, V. K. Mootha, G. E. Sosinsky, M. H. Ellisman, and A. Y. Ting. Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 30:1143–1148, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Miller, M. R., K. J. Robinson, M. D. Cleary, and C. Q. Doe. TU-tagging: cell type-specific RNA isolation from intact complex tissues. Nat. Methods 6:439–441, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Milner, E., E. Barnea, I. Beer, and A. Admon. The turnover kinetics of major histocompatibility complex peptides of human cancer cells. Mol. Cell. Proteomics 5:357–365, 2006.

    Article  CAS  PubMed  Google Scholar 

  54. Mitulovíc, G., and K. Mechtler. HPLC techniques for proteomics analysis-a short overview of latest developments. Brief. Funct. Genomics Proteomics 5:249–260, 2006.

    Article  Google Scholar 

  55. Mosteller, R., R. Goldstein, and K. Nishimoto. Metabolism of individual proteins in exponentially growing Escherichia coli. J. Biol. Chem. 255:2524–2532, 1980.

    CAS  PubMed  Google Scholar 

  56. Nessen, M. A., G. Kramer, J Back, J. M. Baskin, L. E. J. Smeenk, L. J. de Koning, J. H. van Maarseveen, L. de Jong, C. R. Bertozzi, H. Hiemstra, and C. G. de Koster. Selective enrichment of azide-containing peptides from complex mixtures. J. Proteome Res. 8:3702–3711, 2009.

    Google Scholar 

  57. Ngo, J. T., B. M. Babin, J. A. Champion, E. M. Schuman, and D. A. Tirrell. State-selective metabolic labeling of cellular proteins. ACS Chem. Biol. 7:1326–1330, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Ngo, J. T., E. M. Schuman, and D. A. Tirrell. Mutant methionyl-tRNA synthetase from bacteria enables site-selective N-terminal labeling of proteins expressed in mammalian cells. Proc. Natl. Acad. Sci. USA 110:4992–4997, 2013.

    Article  CAS  PubMed  Google Scholar 

  59. Ngo, J. T., J. A. Champion, A. Mahdavi, I. C. Tanrikulu, K. E. Beatty, R. E. Conner, T. H. Yoo, D. C. Dieterich, E. M. Schuman, and D. A. Tirrell. Cell-selective metabolic labeling of proteins. Nat. Chem. Biol. 5:715–717, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Olsen, J. V., S.-E. Ong, and M. Mann. Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 3:608–614, 2004.

    Article  CAS  PubMed  Google Scholar 

  61. Ong, S.-E., and M. Mann. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1:2650–2660, 2007.

    Article  Google Scholar 

  62. Patron, J. P., A. Fendler, M. Bild, U. Jung, H. Müller, M. Ø. Arntzen, C. Piso, C. Stephan, B. Thiede, H.-J. Mollenkopf, K. Jung, S. H. E. Kaufmann, and J. Schreiber. MiR-133b targets antiapoptotic genes and enhances death receptor-induced apoptosis. PLOS ONE 7:e35, 345, 2012.

    Google Scholar 

  63. Picotti, P., B. Bodenmiller, L. N. Mueller, B. Domon, and R. Aebersold. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 138:795–806, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Picotti, P., M. Clément-Ziza, H. Lam, D. S. Campbell, A. Schmidt, E. W. Deutsch, H. Röst, Z. Sun, O. Rinner, L. Reiter, Q. Shen, J. J. Michaelson, A. Frei, S. Alberti, U. Kusebauch, B. Wollscheid, R. L. Moritz, A. Beyer, and R. Aebersold. A complete mass-spectrometric map of the yeast proteome applied to quantitative trait analysis. Nature 494:266–270, 2013.

    Article  CAS  PubMed  Google Scholar 

  65. Pratt, J. M., J. Petty, I. Riba-Garcia, D. H. Robertson, S. J. Gaskell, S. G. Oliver, and R. J. Beynon. Dynamics of protein turnover, a missing dimension in proteomics. Mol. Cell. Proteomics 1:579–591, 2002.

    Article  CAS  PubMed  Google Scholar 

  66. Prescher, J., and C. Bertozzi. Chemistry in living systems. Nat. Chem. Biol. 1:13–21, 2005.

    Article  CAS  PubMed  Google Scholar 

  67. Rabani, M., J. Z. Levin, L. Fan, X. Adiconis, R. Raychowdhury, M. Garber, A. Gnirke, C. Nusbaum, N. Hacohen, N. Friedman, I. Amit, and A. Regev. Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat. Biotechnol. 29:436–442, 2011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Ramsköld, D., S. Luo, Y. C. Wang, R. Li, Q. Deng, O. R. Faridani, G. A. Daniels, I. Khrebtukova, J. F. Loring, L. C. Laurent, G. P. Schroth, and R. Sandberg. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol. 30:777–782, 2012.

    Article  PubMed Central  PubMed  Google Scholar 

  69. Rappsilber, J., and M. Mann. What does it mean to identify a protein in proteomics? Trends Biochem. Sci. 27:74–78, 2002.

    Article  CAS  PubMed  Google Scholar 

  70. Rechavi, O., M. Kalman, Y. Fang, H. Vernitsky, J. Jacob-Hirsch, L. J. Foster, Y. Kloog, and I. Goldstein. Trans-SILAC: sorting out the non-cell-autonomous proteome. Nat. Methods 7:923–927, 2010.

    Article  CAS  PubMed  Google Scholar 

  71. Rhee, H.-W., P. Zou, N. D. Udeshi, J. D. Martell, V. K. Mootha, S. A. Carr, and A. Y. Ting. Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339:1328–1331, 2013.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  72. Rostovtsev, V., L. Green, V. Fokin, and K. Sharpless. A stepwise Huisgen cycloaddition process: copper(I)-catalyzed regioselective ligation of azides and terminal alkynes. Angew. Chem. Int. Ed. 41:2596–2599, 2002.

    Article  CAS  Google Scholar 

  73. Sadygov, R. G., D. Cociorva, and J. R. Yates, III. Large-scale database searching using tandem mass spectra: looking up the answer in the back of the book. Nat. Methods 1:195–202, 2004.

    Article  CAS  PubMed  Google Scholar 

  74. Saxon, E., and C. Bertozzi. Cell surface engineering by a modified Staudinger reaction. Science 287:2007–2010, 2000.

    Article  CAS  PubMed  Google Scholar 

  75. Schwanhäusser, B., M. Gossen, G. Dittmar, and M. Selbach. Global analysis of cellular protein translation by pulsed SILAC. Proteomics 9:205–209, 2009.

    Article  PubMed  Google Scholar 

  76. Schwanhäusser, B., D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, and M. Selbach. Global quantification of mammalian gene expression control. Nature 473:337–342, 2011.

    Article  PubMed  Google Scholar 

  77. Selbach, M., B. Schwanhäusser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58–63, 2008.

    Article  CAS  PubMed  Google Scholar 

  78. Steen, H., and M. Mann. The abc’s (and xyz’s) of peptide sequencing. Nat. Rev. Mol. Cell Biol. 5:699–711, 2004.

    Article  CAS  PubMed  Google Scholar 

  79. Steiner, F. A., P. B. Talbert, S. Kasinathan, R. B. Deal, and S. Henikoff. Cell-type-specific nuclei purification from whole animals for genome-wide expression and chromatin profiling. Genome Res. 22:766–777, 2012.

    Article  CAS  PubMed  Google Scholar 

  80. Sury, M. D., J. X. Chen, and M. Selbach. The SILAC fly allows for accurate protein quantification in vivo. Mol. Cell. Proteomics 9:2173–2183, 2010.

    Article  CAS  PubMed  Google Scholar 

  81. Szychowski, J., A. Mahdavi, J. J. L. Hodas, J. D. Bagert, J. T. Ngo, P. Landgraf, D. C. Dieterich, E. M. Schuman, and D. A. Tirrell. Cleavable biotin probes for labeling of biomolecules via azide-alkyne cycloaddition. J. Am. Chem. Soc. 132:18351–18360, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Taniguchi, Y., P. J. Choi, G. W. Li, H. Chen, M. Babu, J. Hearn, A. Emili, and X. S. Xie. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329:533–538, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Tanrikulu, I. C., E. Schmitt, Y. Mechulam, W. A. Goddard, III, and D. A. Tirrell. Discovery of Escherichia coli methionyl-tRNA synthetase mutants for efficient labeling of proteins with azidonorleucine in vivo. Proc. Natl. Acad. Sci. USA 106:15285–15290, 2009.

    Article  CAS  PubMed  Google Scholar 

  84. Tcherkezian, J., P. A. Brittis, F. Thomas, P. P. Roux, and J. G. Flanagan. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141:632–644, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Thingholm, T. E., O. N. Jensen, and M. R. Larsen. Analytical strategies for phosphoproteomics. Proteomics 9:1451–1468, 2009.

    Article  CAS  PubMed  Google Scholar 

  86. Tomlinson, E., N. Palaniyappan, D. Tooth, and R. Layfield. Methods for the purification of ubiquitinated proteins. Proteomics 7:1016–1022, 2007.

    Article  CAS  PubMed  Google Scholar 

  87. Tornoe, C. W., C. Christensen, and M. Meldal. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 67:3057–3064, 2002.

    Article  CAS  PubMed  Google Scholar 

  88. Truong, F., T. H. Yoo, T. J. Lampo, and D. A. Tirrell. Two-strain, cell-selective protein labeling in mixed bacterial cultures. J. Am. Chem. Soc. 134:8551–8556, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  89. Vogel, C., and E. M. Marcotte. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13:227–232, 2012.

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Vogel, C., S. Abreu Rde, D. Ko, S. Y. Le, B. A. Shaprio, S. C. Burns, D. Sandhu, D. R. Boutz, E. M. Marcotte, and L. O. Penalva. Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol. Syst. Biol. 6:400, 2010.

    Google Scholar 

  91. Wang, Z., M. Gerstein, and M. Snyder. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10:57–63, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  92. Wiese, S., K. A. Reidegeld, H. E. Meyer, and B. Warscheid. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics 7:340–350, 2006.

    Article  Google Scholar 

  93. Yates, J. R., C. I. Ruse, and A. Nakorchevsky. Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng. 11:49–79, 2009.

    Article  CAS  PubMed  Google Scholar 

  94. Yoon, B. C., H. Jung, A. Dwivedy, C. M. O’Hare, K. Zivraj, and C. E. Holt. Local translation of extranuclear lamin B promotes axon maintenance. Cell 148:752–764, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  95. Zhang, L., H. Zhao, B. S. Blagg, and R. T. Dobrowsky. C-terminal heat shock protein 90 inhibitor decreases hyperglycemia-induced oxidative stress and improves mitochondrial bioenergetics in sensory neurons. J. Proteome Res. 11:2581–2593, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  96. Zhang, M. M., L. K. Tsou, G. Charron, A. S. Raghavan, and H. C. Hang. Tandem fluorescence imaging of dynamic S-acylation and protein turnover. Proc. Natl. Acad. Sci. USA 107:8627–8632, 2010.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Work at Caltech on non-canonical amino acid tagging is supported by National Institutes of Health grant NIH R01 GM062523 and by the Institute for Collaborative Biotechnologies through grant W911NF-09-0001 from U.S. Army Research Office.

Author information

Authors and Affiliations

  1. Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, CA, USA

    Kai P. Yuet & David A. Tirrell

Authors
  1. Kai P. Yuet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. Tirrell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David A. Tirrell.

Additional information

Associate Editor Robert Nerem oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yuet, K.P., Tirrell, D.A. Chemical Tools for Temporally and Spatially Resolved Mass Spectrometry-Based Proteomics. Ann Biomed Eng 42, 299–311 (2014). https://doi.org/10.1007/s10439-013-0878-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-013-0878-3

Keywords

Search

Navigation